SAR11 is a group of small, carbon-oxidizing bacteria that reach a global estimated population size of 2.4×10
28
cells-approximately 25% of all plankton. They are found throughout the oceans but reach ...their largest numbers in stratified, oligotrophic gyres, which are an expanding habitat in the warming oceans. SAR11 likely had a Precambrian origin and, over geological time, evolved into the niche of harvesting labile, low-molecular-weight dissolved organic matter (DOM). SAR11 cells are minimal in size and complexity, a phenomenon known as streamlining that is thought to benefit them by lowering the material costs of replication and maximizing transport functions that are essential to competition at ultralow nutrient concentrations. One of the surprises in SAR11 metabolism is their ability to both oxidize and produce a variety of volatile organic compounds that can diffuse into the atmosphere. SAR11 cells divide slowly and lack many forms of regulation commonly used by bacterial cells to adjust to changing environmental conditions. As a result of genome reduction, they require an unusual range of nutrients, which leads to complex biochemical interactions with other plankton. The study of SAR11 is providing insight into the biogeochemistry of labile DOM and is affecting microbiology beyond marine science by providing a model for understanding the evolution and function of streamlined cells.
Whether a small cell, a small genome or a minimal set of chemical reactions with self-replicating properties, simplicity is beguiling. As Leonardo da Vinci reportedly said, 'simplicity is the ...ultimate sophistication'. Two diverging views of simplicity have emerged in accounts of symbiotic and commensal bacteria and cosmopolitan free-living bacteria with small genomes. The small genomes of obligate insect endosymbionts have been attributed to genetic drift caused by small effective population sizes (Ne). In contrast, streamlining theory attributes small cells and genomes to selection for efficient use of nutrients in populations where Ne is large and nutrients limit growth. Regardless of the cause of genome reduction, lost coding potential eventually dictates loss of function. Consequences of reductive evolution in streamlined organisms include atypical patterns of prototrophy and the absence of common regulatory systems, which have been linked to difficulty in culturing these cells. Recent evidence from metagenomics suggests that streamlining is commonplace, may broadly explain the phenomenon of the uncultured microbial majority, and might also explain the highly interdependent (connected) behavior of many microbial ecosystems. Streamlining theory is belied by the observation that many successful bacteria are large cells with complex genomes. To fully appreciate streamlining, we must look to the life histories and adaptive strategies of cells, which impose minimum requirements for complexity that vary with niche.
Changing tastes in marine microbe food webs
Protists are single-celled organisms complete with nuclei, organelles, and symbionts, and possess a multiplicity of physiological talents. They are ...ubiquitous, abundant, and often neglected by science. Worden
et al.
review the challenges of understanding the role protists play in geochemical cycling in the oceans. These organisms can photosynthesize like plants, graze on bacteria and archaea, parasitize each other and bigger creatures, have sex, and sometimes do all these things serially as conditions change. Their activities may have a significant influence on carbon cycling, and research efforts need to be amplified to understand their functional importance in marine ecosystems.
Science
, this issue
10.1126/science.1257594
BACKGROUND
Marine ecosystems are composed of a diverse array of life forms, the majority of which are unicellular—archaea, bacteria, and eukaryotes. The power of these microbes to process carbon, shape Earth’s atmosphere, and fuel marine food webs has been established over the past 40 years. The marine biosphere is responsible for approximately half of global primary production, rivaling that of land plants. Unicellular eukaryotes (protists) are major contributors to this ocean productivity. In addition to photosynthetic growth, protists exhibit a range of other trophic modes, including predation, mixotrophy (a combination of photosynthetic and predatory-based nutrition), parasitism, symbiosis, osmotrophy, and saprotrophy (wherein extracellular enzymes break down organic matter to smaller compounds that are then transported into the cell by osmotrophy).
ADVANCES
Sensitive field approaches have illuminated the enormous diversity of protistan life (much of it uncultured) and, coupled with activity measurements, are leading to hypotheses about their ecological roles. In parallel, large-scale sequencing projects are providing fundamental advances in knowledge of genome/gene composition, especially among photosynthetic lineages, many of which are complex amalgams derived from multiple endosymbiotic mergers. Marine protists have yielded insight into basic biology, evolution, and molecular machineries that control organismal responses to the environment. These studies reveal tightly controlled signaling and transcriptional regulation as well as responses to limitation of resources such as iron, nitrogen, and vitamins, and offer understanding of animal and plant evolution. With the formulation of better computational approaches, hypotheses about interactions and trophic exchanges are becoming more exact and modelers more assertive at integrating different data types. At the same time, the impacts of climate change are being reported in multiple systems, of which polar environments are the touchstone of change.
OUTLOOK
Driven by the need to translate the biology of cells into processes at global scales, researchers must bring the conceptual framework of systems biology into bigger “ecosystems biology” models that broadly capture the geochemical activities of interacting plankton networks. Existing data show that protists are major components of marine food webs, but deducing and quantifying their ecosystem linkages and the resulting influences on carbon cycling is difficult. Genome-based functional predictions are complicated by the importance of cellular structures and flexible behaviors in protists, which are inherently more difficult to infer than the biochemical pathways typically studied in prokaryotes. Alongside the plethora of genes of unknown function, manipulable genetic systems are rare for marine protists. The development of genetic systems and gene editing for diverse, ecologically important lineages, as well as innovative tools for preserving microbe-microbe interactions during sampling, for visual observation, and for quantifying biogeochemical transformations, are critical but attainable goals. These must be implemented in both field work and laboratory physiology studies that examine multiple environmental factors. Expanding genome functional predictions to identify the molecular underpinnings of protistan trophic modes and realistically constrain metabolism will position the field to build reliable cell systems biology models and link these to field studies. By factoring in true complexities, we can capture key elements of protistan interactions for assimilation into more predictive global carbon cycle models.
Global biogeochemical and ecological models rely on understanding organismal biology and the interactions occurring in marine microbial food webs.
Protists have multifarious roles from the sunlit surface ocean to leagues below. Understanding of protistan behaviors and adaptability lags far behind knowledge of evolutionary processes that have shaped their genomes. As such, microbial mediation of carbon fluxes and specific interactions remain ill-resolved and predictive capabilities are still weak. Strategies to narrow this gap involve iteration between experimental and observational field studies, controlled laboratory experiments, systems biology approaches that preserve cellular structures and behaviors using relevant model taxa, and computational approaches.
The profound influence of marine plankton on the global carbon cycle has been recognized for decades, particularly for photosynthetic microbes that form the base of ocean food chains. However, a comprehensive model of the carbon cycle is challenged by unicellular eukaryotes (protists) having evolved complex behavioral strategies and organismal interactions that extend far beyond photosynthetic lifestyles. As is also true for multicellular eukaryotes, these strategies and their associated physiological changes are difficult to deduce from genome sequences or gene repertoires—a problem compounded by numerous unknown function proteins. Here, we explore protistan trophic modes in marine food webs and broader biogeochemical influences. We also evaluate approaches that could resolve their activities, link them to biotic and abiotic factors, and integrate them into an ecosystems biology framework.
Seasonality in Ocean Microbial Communities Giovannoni, Stephen J.; Vergin, Kevin L.
Science (American Association for the Advancement of Science),
02/2012, Letnik:
335, Številka:
6069
Journal Article
Recenzirano
Ocean warming occurs every year in seasonal cycles that can help us to understand long-term responses of plankton to climate change. Rhythmic seasonal patterns of microbial community turnover are ...revealed when high-resolution measurements of microbial plankton diversity are applied to samples collected in lengthy time series. Seasonal cycles in microbial plankton are complex, but the expansion of fixed ocean stations monitoring long-term change and the development of automated instrumentation are providing the time-series data needed to understand how these cycles vary across broad geographical scales. By accumulating data and using predictive modeling, we gain insights into changes that will occur as the ocean surface continues to warm and as the extent and duration of ocean stratification increase. These developments will enable marine scientists to predict changes in geochemical cycles mediated by microbial communities and to gauge their broader impacts.
Previous studies have demonstrated that Candidatus Pelagibacter ubique, a member of the SAR11 clade, constitutively expresses proteorhodopsin (PR) proteins that can function as light-dependent proton ...pumps. However, exposure to light did not significantly improve the growth rate or final cell densities of SAR11 isolates in a wide range of conditions. Thus, the ecophysiological role of PR in SAR11 remained unresolved. We investigated a range of cellular properties and here show that light causes dramatic changes in physiology and gene expression in Cand. P. ubique cells that are starved for carbon, but provides little or no advantage during active growth on organic carbon substrates. During logarithmic growth there was no difference in oxygen consumption by cells in light versus dark. Energy starved cells respired endogenous carbon in the dark, becoming spheres that approached the minimum predicted size for cells, and produced abundant pili. In the light, energy starved cells maintained size, ATP content, and higher substrate transport rates, and differentially expressed nearly 10% of their genome. These findings show that PR is a vital adaptation that supports Cand. P. ubique metabolism during carbon starvation, a condition that is likely to occur in the extreme conditions of ocean environments.
Bacteria in the class Alphaproteobacteria have a wide variety of lifestyles and physiologies. They include pathogens of humans and livestock, agriculturally valuable strains, and several highly ...abundant marine groups. The ancestor of mitochondria also originated in this clade. Despite significant effort to investigate the phylogeny of the Alphaproteobacteria with a variety of methods, there remains considerable disparity in the placement of several groups. Recent emphasis on phylogenies derived from multiple protein-coding genes remains contentious due to disagreement over appropriate gene selection and the potential influences of systematic error. We revisited previous investigations in this area using concatenated alignments of the small and large subunit (SSU and LSU) rRNA genes, as we show here that these loci have much lower GC bias than whole genomes. This approach has allowed us to update the canonical 16S rRNA gene tree of the Alphaproteobacteria with additional important taxa that were not previously included, and with added resolution provided by concatenating the SSU and LSU genes. We investigated the topological stability of the Alphaproteobacteria by varying alignment methods, rate models, taxon selection and RY-recoding to circumvent GC content bias. We also introduce RYMK-recoding and show that it avoids some of the information loss in RY-recoding. We demonstrate that the topology of the Alphaproteobacteria is sensitive to inclusion of several groups of taxa, but it is less affected by the choice of alignment and rate methods. The majority of topologies and comparative results from Approximately Unbiased tests provide support for positioning the Rickettsiales and the mitochondrial branch within a clade. This composite clade is a sister group to the abundant marine SAR11 clade (Pelagibacterales). Furthermore, we add support for taxonomic assignment of several recently sequenced taxa. Accordingly, we propose three subclasses within the Alphaproteobacteria: the Caulobacteridae, the Rickettsidae, and the Magnetococcidae.
The SAR11 Alphaproteobacteria are the most abundant heterotrophs in the oceans and are believed to play a major role in mineralizing marine dissolved organic carbon. Their genomes are among the ...smallest known for free-living heterotrophic cells, raising questions about how they successfully utilize complex organic matter with a limited metabolic repertoire. Here we show that conserved genes in SAR11 subgroup Ia (Candidatus Pelagibacter ubique) genomes encode pathways for the oxidation of a variety of one-carbon compounds and methyl functional groups from methylated compounds. These pathways were predicted to produce energy by tetrahydrofolate (THF)-mediated oxidation, but not to support the net assimilation of biomass from C1 compounds. Measurements of cellular ATP content and the oxidation of (14)C-labeled compounds to (14)CO(2) indicated that methanol, formaldehyde, methylamine, and methyl groups from glycine betaine (GBT), trimethylamine (TMA), trimethylamine N-oxide (TMAO), and dimethylsulfoniopropionate (DMSP) were oxidized by axenic cultures of the SAR11 strain Ca. P. ubique HTCC1062. Analyses of metagenomic data showed that genes for C1 metabolism occur at a high frequency in natural SAR11 populations. In short term incubations, natural communities of Sargasso Sea microbial plankton expressed a potential for the oxidation of (14)C-labeled formate, formaldehyde, methanol and TMAO that was similar to cultured SAR11 cells and, like cultured SAR11 cells, incorporated a much larger percentage of pyruvate and glucose (27-35%) than of C1 compounds (2-6%) into biomass. Collectively, these genomic, cellular and environmental data show a surprising capacity for demethylation and C1 oxidation in SAR11 cultures and in natural microbial communities dominated by SAR11, and support the conclusion that C1 oxidation might be a significant conduit by which dissolved organic carbon is recycled to CO(2) in the upper ocean.
The history of microbial evolution in the oceans is probably as old as the history of life itself. In contrast to terrestrial ecosystems, microorganisms are the main form of biomass in the oceans, ...and form some of the largest populations on the planet. Theory predicts that selection should act more efficiently in large populations. But whether microbial plankton populations harbour organisms that are models of adaptive sophistication remains to be seen. Genome sequence data are piling up, but most of the key microbial plankton clades have no cultivated representatives, and information about their ecological activities is sparse.
Deep-ocean regions beyond the reach of sunlight contain an estimated 615 Pg of dissolved organic matter (DOM), much of which persists for thousands of years. It is thought that bacteria oxidize DOM ...until it is too dilute or refractory to support microbial activity. We analyzed five single-amplified genomes (SAGs) from the abundant SAR202 clade of dark-ocean bacterioplankton and found they encode multiple families of paralogous enzymes involved in carbon catabolism, including several families of oxidative enzymes that we hypothesize participate in the degradation of cyclic alkanes. The five partial genomes encoded 152 flavin mononucleotide/F420-dependent monooxygenases (FMNOs), many of which are predicted to be type II Baeyer-Villiger monooxygenases (BVMOs) that catalyze oxygen insertion into semilabile alicyclic alkanes. The large number of oxidative enzymes, as well as other families of enzymes that appear to play complementary roles in catabolic pathways, suggests that SAR202 might catalyze final steps in the biological oxidation of relatively recalcitrant organic compounds to refractory compounds that persist.
Carbon in the ocean is massively sequestered in a complex mixture of biologically refractory molecules that accumulate as the chemical end member of biological oxidation and diagenetic change. However, few details are known about the biochemical machinery of carbon sequestration in the deep ocean. Reconstruction of the metabolism of a deep-ocean microbial clade, SAR202, led to postulation of new biochemical pathways that may be the penultimate stages of DOM oxidation to refractory forms that persist. These pathways are tied to a proliferation of oxidative enzymes. This research illuminates dark-ocean biochemistry that is broadly consequential for reconstructing the global carbon cycle.
THE UNCULTURED MICROBIAL MAJORITY Rappé, Michael S; Giovannoni, Stephen J
Annual review of microbiology,
01/2003, Letnik:
57, Številka:
1
Journal Article
Recenzirano
Since the delineation of 12 bacterial phyla by comparative phylogenetic
analyses of 16S ribosomal RNA in 1987 knowledge of microbial diversity has
expanded dramatically owing to the sequencing of ...ribosomal RNA genes cloned
from environmental DNA. Currently, only 26 of the approximately 52 identifiable
major lineages, or phyla, within the domain Bacteria have cultivated
representatives. Evidence from field studies indicates that many of the
uncultivated phyla are found in diverse habitats, and some are extraordinarily
abundant. In some important environments, including seawater, freshwater, and
soil, many biologically and geochemically important organisms are at best only
remotely related to any strain that has been characterized by phenotype or by
genome sequencing. Genome sequence information that would allow ribosomal RNA
gene trees to be related to broader patterns in microbial genome evolution is
scant, and therefore microbial diversity remains largely unexplored
territory.
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